Mechanisms of ovarian cancer metastasis: Biochemical pathways

International Journal of Molecular Sciences

Volumn 13, Issue 9, 2012, Pages 11705-11717

  Nakayama, Kentaro ^a   Nakayama, Naomi ^a   Katagiri, Hiroshi ^a   Miyazaki, Kohji ^a  

^a SHIMANE UNIVERSITY FACULTY OF MEDICINE   (Japan)

Author keywords

Cancer; EMT; Metastasis suppressor gene; Tumor microenvironment

Indexed keywords

BREAST CANCER METASTASIS SUPPRESSOR 1; CD82 ANTIGEN; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 54; METASTIN; MICRORNA; NUCLEOSIDE DIPHOSPHATE KINASE NM23; OVARIAN CANCER G PROTEIN COUPLED RECEPTOR 1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ANOIKIS; APOPTOSIS; BIOCHEMISTRY; BREAST CANCER METASTASIS SUPPRESSOR 1 GENE; CANCER CHEMOTHERAPY; CANCER GENETICS; CANCER RESISTANCE; E CADHERIN GENE; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE FUNCTION; HUMAN; KAI1 GENE; KISS1 GENE; KISS1 RECEPTOR GENE; METASTASIS; NM23 GENE; NONHUMAN; OVARIAN CANCER G PROTEIN COUPLED RECEPTOR GENE; OVARY CANCER; RECEPTOR GENE; REVIEW; TUMOR MICROENVIRONMENT; TUMOR SUPPRESSOR GENE;

EID: 84866937603     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms130911705     Document Type: Review

References (67)

1. Cook, L.M.; Hurst, D.R.; Welch, D.R. Metastasis suppressors and the tumor microenvironment. Semin. Cancer Biol. 2011, 21, 113-122.
2. Thiolloy, S.; Rinker-Schaeffer, C.W. Thinking outside the box: Using metastasis suppressors as molecular tools. Semin. Cancer Biol. 2011, 21, 89-98.
3. Youn, B.S.; Kim, D.S.; Kim, J.W.; Kim, Y.T.; Kang, S.; Cho, N.H. NM23 as a prognostic biomarker in ovarian serous carcinoma. Mod. Pathol. 2008, 21, 885-892.
4. Prentice, L.M.; Klausen, C.; Kalloger, S.; Kobel, M.; McKinney, S.; Santos, J.L.; Kenney, C.; Mehl, E.; Gilks, C.B.; Leung, P. et al. Kisspeptin and GPR54 immunoreactivity in a cohort of 518 patients defines favorable prognosis and clear cell subtype in ovarian carcinoma. BMC Med. 2007, 5, 33.
5. Hata, K.; Dhar, D.K.; Watanabe, Y.; Nakai, H.; Hoshiai, H. Expression of metastin and a G-protein-coupled receptor (AXOR12) in epithelial ovarian cancer. Eur. J. Cancer 2007, 43, 1452-1459.
6. Houle, C.D.; Ding, X.Y.; Foley, J.F.; Afshari, C.A.; Barrett, J.C.; Davis, B.J. Loss of expression and altered localization of KAI1 and CD9 protein are associated with epithelial ovarian cancer progression. Gynecol. Oncol. 2002, 86, 69-78.
7. Ruseva, Z.; Geiger, P.X.; Hutzler, P.; Kotzsch, M.; Luber, B.; Schmitt, M.; Gross, E.; Reuning, U. Tumor suppressor KAI1 affects integrin alphavbeta3-mediated ovarian cancer cell adhesion, motility, and proliferation. Exp. Cell Res. 2009, 315, 1759-1771.
8. Kim, G.; Davidson, B.; Henning, R.; Wang, J.; Yu, M.; Annunziata, C.; Hetland, T.; Kohn, E.C. Adhesion molecule protein signature in ovarian cancer effusions is prognostic of patient outcome. Cancer 2012, 118, 1543-1553.
9. Ho, C.M.; Cheng, W.F.; Lin, M.C.; Chen, T.C.; Huang, S.H.; Liu, F.S.; Chien, C.C.; Yu, M.H.; Wang, T.Y.; Hsieh, C.Y. Prognostic and predictive values of E-cadherin for patients of ovarian clear cell adenocarcinoma. Int. J. Gynecol.Cancer 2010, 20, 1490-1497.
10. Ren, J.; Zhang, L. Effects of ovarian cancer G protein coupled receptor 1 on the proliferation, migration, and adhesion of human ovarian cancer cells. Chin. Med. J. (Engl.) 2011, 124, 1327-1332.
11. Zhang, S.; Lin, Q.D.; Di, W. Suppression of human ovarian carcinoma metastasis by the metastasis-suppressor gene, BRMS1. Int. J. Gynecol. Cancer 2006, 16, 522-531.
12. Sheng, X.J.; Zhou, Y.Q.; Song, Q.Y.; Zhou, D.M.; Liu, Q.C. Loss of breast cancer metastasis suppressor 1 promotes ovarian cancer cell metastasis by increasing chemokine receptor 4 expression. Oncol. Rep. 2012, 27, 1011-1018.
13. Yeasmin, S.; Nakayama, K.; Rahman, M.T.; Rahman, M.; Ishikawa, M.; Katagiri, A.; Iida, K.; Nakayama, N.; Miyazaki, K. Loss of MKK4 expression in ovarian cancer: A potential role for the epithelial to mesenchymal transition. Int. J. Cancer 2011, 128, 94-104.
14. Nakayama, K.; Nakayama, N.; Davidson, B.; Katabuchi, H.; Kurman, R.J.; Velculescu, V.E.; Shih Ie, M.; Wang, T.L. Homozygous deletion of MKK4 in ovarian serous carcinoma. Cancer Biol. Ther. 2006, 5, 630-634.
15. Steeg, P.S.; Bevilacqua, G.; Kopper, L.; Thorgeirsson, U.P.; Talmadge, J.E.; Liotta, L.A.; Sobel, M.E. Evidence for a novel gene associated with low tumor metastatic potential. J. Natl. Cancer Inst. 1988, 80, 200-204.
16. Kantor, J.D.; McCormick, B.; Steeg, P.S.; Zetter, B.R. Inhibition of cell motility after nm23 transfection of human and murine tumor cells. Cancer Res. 1993, 53, 1971-1973.
17. Lee, H.Y.; Lee, H. Inhibitory activity of nm23-H1 on invasion and colonization of human prostate carcinoma cells is not mediated by its NDP kinase activity. Cancer Lett. 1999, 145, 93-99.
18. Kotani, M.; Detheux, M.; Vandenbogaerde, A.; Communi, D.; Vanderwinden, J.M.; Le Poul, E.; Brézillon, S.; Tyldesley, R.; Suarez-Huerta, N.; Vandeput, F. et al. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J. Biol. Chem. 2001, 276, 34631-34636.
19. Ohtaki, T.; Shintani, Y.; Honda, S.; Matsumoto, H.; Hori, A.; Kanehashi, K.; Terao, Y.; Kumano, S.; Takatsu, Y.; Masuda, Y. et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001, 411, 613-617.
20. Stipp, C.S.; Kolesnikova, T.V.; Hemler, M.E. Functional domains in tetraspanin proteins. Trends Biochem. Sci. 2003, 28, 106-112.
21. Voulgari, A.; Pintzas, A. Epithelial-mesenchymal transition in cancer metastasis: Mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim. Biophys. Acta 2009, 1796, 75-90.
22. Singh, L.S.; Berk, M.; Oates, R.; Zhao, Z.; Tan, H.; Jiang, Y.; Zhou, A.; Kirmani, K.; Steinmetz, R.; Lindner, D.; et al. Ovarian cancer G protein-coupled receptor 1, a new metastasis suppressor gene in prostate cancer. J. Natl. Cancer Inst. 2007, 99, 1313-1327.
23. Kalluri, R.; Weinberg, R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119, 1420-1428.
24. Terauchi, M.; Kajiyama, H.; Yamashita, M.; Kato, M.; Tsukamoto, H.; Umezu, T.; Hosono, S.; Yamamoto, E.; Shibata, K.; Ino, K. et al. Possible involvement of TWIST in enhanced peritoneal metastasis of epithelial ovarian carcinoma. Clin. Exp. Metastasis 2007, 24, 329-339.
25. Nakayama, K.; Nakayama, N.; Wang, T.L.; Shih Ie, M. NAC-1 controls cell growth and survival by repressing transcription of Gadd45GIP1, a candidate tumor suppressor. Cancer Res. 2007, 67, 8058-8064.
26. Nakayama, K.; Rahman, M.T.; Rahman, M.; Yeasmin, S.; Ishikawa, M.; Katagiri, A.; Iida, K.; Nakayama, N.; Miyazaki, K. Biological role and prognostic significance of NAC1 in ovarian cancer. Gynecol. Oncol. 2010, 119, 469-478.
27. Nakayama, K.; Nakayama, N.; Miyazaki, K. Development of a novel ovarian cancer molecular target therapy against cancer-related transcriptional factor, NAC1. J. Obstet. Gynaecol. Res. 2012, doi: 10.1111/j.1447-0756.2012.01946.x.
28. Frisch, S.M.; Francis, H. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 1994, 124, 619-626.
29. Cheng, K.W.; Lahad, J.P.; Kuo, W.L.; Lapuk, A.; Yamada, K.; Auersperg, N.; Liu, J.; Smith-McCune, K.; Lu, K.H.; Fishman, D. et al. The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers. Nat. Med. 2004, 10, 1251-1256.
30. Kajiyama, H.; Shibata, K.; Terauchi, M.; Yamashita, M.; Ino, K.; Nawa, A.; Kikkawa, F. Chemoresistance to paclitaxel induces epithelial-mesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells. Int. J. Oncol. 2007, 31, 277-283.
31. Sood, A.K.; Armaiz-Pena, G.N.; Halder, J.; Nick, A.M.; Stone, R.L.; Hu, W.; Carroll, A.R.; Spannuth, W.A.; Deavers, M.T.; Allen, J.K. et al. Adrenergic modulation of focal adhesion kinase protects human ovarian cancer cells from anoikis. J. Clin. Invest. 2010, 120, 1515-1523.
32. Filipowicz, W.; Bhattacharyya, S.N.; Sonenberg, N. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat. Rev. Genet. 2008, 9, 102-114.
33. Tavazoie, S.F.; Alarcón, C.; Oskarsson, T.; Padua, D.; Wang, Q.; Bos, P.D.; Gerald, W.L.; Massagué, J. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008, 451, 147-152.
34. Park, S.M.; Gaur, A.B.; Lengyel, E.; Peter, M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008, 22, 894-907.
35. Huang, Q.; Gumireddy, K.; Schrier, M.; le Sage, C.; Nagel, R.; Nair, S.; Egan, D.A.; Li, A.; Huang, G.; Klein-Szanto, A.J. et al. The microRNAs miR-373 and miR-520c promote tumor invasion and metastasis. Nat. Cell Biol. 2008, 10, 202-210.
36. Mateescu, B.; Batista, L.; Cardon, M.; Gruosso, T.; de Feraudy, Y.; Mariani, O.; Nicolas, A.; Meyniel, J.P.; Cottu, P.; Sastre-Garau, X. et al. miR-141 and miR-200a act on ovarian tumorigenesis by controlling oxidative stress response. Nat. Med. 2011, 17, 627-635.
37. Schauer, I.G.; Sood, A.K.; Mok, S.; Liu, J. Cancer-associated fibroblasts and their putative role in potentiating the initiation and development of epithelial ovarian cancer. Neoplasia 2011, 13, 393-405.
38. Cai, J.; Tang, H.; Xu, L.; Wang, X.; Yang, C.; Ruan, S.; Guo, J.; Hu, S.; Wang, Z. Fibroblasts in omentum activated by tumor cells promote ovarian cancer growth, adhesion and invasiveness. Carcinogenesis 2012, 33, 20-29.
39. Cirri, P.; Chiarugi, P. Cancer-associated-fibroblasts and tumor cells: A diabolic liaison driving cancer progression. Cancer Metastasis Rev. 2012, 31, 195-208.
40. Stagg, J. Mesenchymal stem cells in cancer. Stem. Cell Rev. 2008, 4, 119-124.
41. McLean, K.; Gong, Y.; Choi, Y.; Deng, N.; Yang, K.; Bai, S.; Cabrera, L.; Keller, E.; McCauley, L.; Cho, K.R. et al. Human ovarian carcinoma-associated mesenchymal stem cells regulate cancer stem cells and tumorigenesis via altered BMP production. J. Clin. Invest. 2011, 121, 3206-3219.
42. Cho, K.R.; Shih, I.-M. Ovarian cancer. Annu. Rev. Pathol. 2009, 4, 287-313.
43. Nieman, K.M.; Kenny, H.A.; Penicka, C.V.; Ladanyi, A.; Buell-Gutbrod, R.; Zillhardt, M.R.; Romero, I.L.; Carey, M.S.; Mills, G.B.; Hotamisligil, G.S. et al. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat. Med. 2011, 17, 1498-1503.
44. Corps, A.N.; Sowter, H.M.; Smith, S.K. Hepatocyte growth factor stimulates motility, chemotaxis and mitogenesis in ovarian carcinoma cells expressing high levels of c-met. Int. J. Cancer 1997, 73, 151-155.
45. Orimo, A.; Gupta, P.B.; Sgroi, D.C.; Arenzana-Seisdedos, F.; Delaunay, T.; Naeem, R.; Carey, V.J.; Richardson, A.L.; Weinberg, R.A. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005, 121, 335-348.
46. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474, 609-615.
47. Sato, E.; Olson, S.H.; Ahn, J.; Bundy, B.; Nishikawa, H.; Qian, F.; Jungbluth, A.A.; Frosina, D.; Gnjatic, S.; Ambrosone, C. et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc. Natl. Acad. Sci.USA 2005, 102, 18538-18543.
48. Hamanishi, J.; Mandai, M.; Iwasaki, M.; Okazaki, T.; Tanaka, Y.; Yamaguchi, K.; Higuchi, T.; Yagi, H.; Takakura, K.; Minato, N. et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc. Natl. Acad. Sci. USA 2007, 104, 3360-3365.
49. Scarlett, U.K.; Rutkowski, M.R.; Rauwerdink, A.M.; Fields, J.; Escovar-Fadul, X.; Baird, J.; Cubillos-Ruiz, J.R.; Jacobs, A.C.; Gonzalez, J.L.; Weaver, J. et al. Ovarian cancer progression is controlled by phenotypic changes in dendritic cells. J. Exp. Med. 2012, 209, 495-506.
50. Birner, P.; Schindl, M.; Obermair, A.; Breitenecker, G.; Oberhuber, G. Expression of hypoxia-inducible factor 1alpha in epithelial ovarian tumors: Its impact on prognosis and on response to chemotherapy. Clin. Cancer Res. 2001, 7, 1661-1668.
51. Osada, R.; Horiuchi, A.; Kikuchi, N.; Yoshida, J.; Hayashi, A.; Ota, M.; Katsuyama, Y.; Melillo, G.; Konishi, I. Expression of hypoxia-inducible factor 1alpha, hypoxia-inducible factor 2alpha, and von Hippel-Lindau protein in epithelial ovarian neoplasms and allelic loss of von Hippel-Lindau gene: Nuclear expression of hypoxia-inducible factor 1alpha is an independent prognostic factor in ovarian carcinoma. Hum. Pathol. 2007, 38, 1310-1320.
52. Imai, T.; Horiuchi, A.; Wang, C.; Oka, K.; Ohira, S.; Nikaido, T.; Konishi, I. Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells. Am. J. Pathol. 2003, 163, 1437-1447.
53. Kryczek, I.; Lange, A.; Mottram, P.; Alvarez, X.; Cheng, P.; Hogan, M.; Moons, L.; Wei, S.; Zou, L.; Machelon, V. et al. CXCL12 and vascular endothelial growth factor synergistically induce neoangiogenesis in human ovarian cancers. Cancer Res. 2005, 65, 465-472.
54. Nakayama, K.; Kanzaki, A.; Hata, K.; Katabuchi, H.; Okamura, H.; Miyazaki, K.; Fukumoto, M.; Takebayashi, Y. Hypoxia-inducible factor 1 alpha (HIF-1 alpha) gene expression in human ovarian carcinoma. Cancer Lett. 2002, 176, 215-223.
55. Aruffo, A.; Stamenkovic, I.; Melnick, M.; Underhill, C.B.; Seed, B. CD44 is the principal cell surface receptor for hyaluronate. Cell 1990, 61, 1303-1313.
56. Gardner, M.J.; Catterall, J.B.; Jones, L.M.; Turner, G.A. Human ovarian tumor cells can bind hyaluronic acid via membrane CD44: A possible step in peritoneal metastasis. Clin. Exp. Metastasis 1996, 14, 325-334.
57. Casey, R.C.; Koch, K.A. Oegema, T.R., Jr.; Skubitz, K.M.; Pambuccian, S.E.; Grindle, S.M.; Skubitz, A.P. Establishment of an in vitro assay to measure the invasion of ovarian carcinoma cells through mesothelial cell monolayers. Clin. Exp. Metastasis 2003, 20, 343-356.
58. Cannistra, S.A.; Kansas, G.S.; Niloff, J.; DeFranzo, B.; Kim, Y.; Ottensmeier, C. Binding of ovarian cancer cells to peritoneal mesothelium in vitro is partly mediated by CD44H. Cancer Res. 1993, 53, 3830-3838.
59. Ween, M.P.; Hummitzsch, K.; Rodgers, R.J.; Oehler, M.K.; Ricciardelli, C. Versican induces a pro-metastatic ovarian cancer cell behavior which can be inhibited by small hyaluronan oligosaccharides. Clin. Exp. Metastasis 2010, doi: 10.1007/s10585-010-9363-7.
60. Brabletz, T.; Jung, A.; Spaderna, S.; Hlubek, F.; Kirchner, T. Migrating cancer stem cells-An integrated concept of malignant tumor progression. Nat. Rev. Cancer 2005, 5, 744-749.
61. Meng, E.; Long, B.; Sullivan, P.; McClellan, S.; Finan, M.A.; Reed, E.; Shevde, L.; Rocconi, R.P. CD44+/CD24- ovarian cancer cells demonstrate cancer stem cell properties and correlate to survival. Clin. Exp. Metastasis 2012, doi: 10.1007/s10585-012-9482-4.
62. Lu, C.; Han, H.D.; Mangala, L.S.; Ali-Fehmi, R.; Newton, C.S.; Ozbun, L.; Armaiz-Pena, G.N.; Hu, W.; Stone, R.L.; Munkarah, A. et al. Regulation of tumor angiogenesis by EZH2. Cancer Cell 2010, 18, 185-197.
63. Bauvois, B. New facets of matrix metalloproteinases MMP-2 and MMP-9 as cell surface transducers: Outside-in signaling and relationship to tumor progression. Biochim. Biophys. Acta 2012, 1825, 29-36.
64. Seo, J.M.; Park, S.; Kim, J.H. Leukotriene B4 Receptor-2 promotes invasiveness and metastasis of ovarian cancer cells through signal transducer and activator of transcription 3 (STAT3)-dependent up-regulation of matrix metalloproteinase 2. J. Biol. Chem. 2012, 287, 13840-13849.
65. Sakurai, T.; Kudo, M. Signaling pathways governing tumor angiogenesis. Oncology 2011, 81, 24-29.
66. Zucker, S.; Cao, J.; Chen, W.T. Critical appraisal of the use of matrix metalloproteinase inhibitors in cancer treatment. Oncogene 2000, 19, 6642-6650.
67. Overall, C.M.; Lopez-Otin, C. Strategies for MMP inhibition in cancer: Innovations for the post-trial era. Nat. Rev. Cancer 2002, 2, 657-672.